INTRODUCTION
Rice (Oryza sativa L.) is most important cereal crops in Indonesia. Rice plantation is a rapid changing ecosystem due to the change of activities during cultivation. These activities affect the pest population and also the abundance of their natural enemies in the rice field (Khaliq, Javed, Sohail, &
Sagheer, 2014; Tsutsui, Kobayashi, & Miyashita, 2018). Some of the insect pests that are known to harm the rice plantation are Leucopholis rorida (Fabr.), brown plant hopper Nilaparvata lugens (Stål), rice shoot fly Atherigona oryzae (Malloch), white stem borer Scirpophaga innotata (Walker), and rice bug Leptocorisa oratorius (Thunberg) (Ooi, 2015; Thorburn, 2015).
The increase of Indonesian population has also driven a higher need of rice production, however many rice farmers are still very much dependent on chemical pesticides (Kalsum & Romza, 2013).
The excessive use of chemical pesticides i.e.
insecticides can lead to pest resistance, resurgence, the killing of non-target organisms (such as natural enemies), ground water contamination, change of soil microbial diversity, and risks to human health
(Gill & Garg, 2014). Integrated Pest Management (IPM) strategies have been developed in order to control rice pests. Integrated Pest Management is defined as a holistic strategy to decrease plant pests and diseases using all available and compatible methods, but minimizing the use of chemical pesticides (Matthews, 2003; Stenberg, 2017).
Several methods of pest control which are more environmentally friendly such as biological and mechanical controls, and also botanical pesticides are employed in IPM (Borkhani, Rezvanfar, Fami, & Pouratashi, 2010). The Integrated Pest Management has been adopted formally as the principle of plant protection in Indonesia through the government regulation number 12 in the year 1992. Years before that (the mid-1980s) IPM was introduced to Indonesia as a new crop management approach particularly for rice plantations and developed the Farmer Field School (FFS) model of empowering farmers to make their own decisions regarding management of their rice field. However, FFS was no longer practiced since the late 1990s, and nowadays, rice farmers tend to use pesticides with many negative consequences occur in the field (Thorburn, 2015).
ARTICLE INFO Keywords:
Biological control Food crop Natural enemies Parasitoid Predator Article History:
Received: February 13, 2019 Accepted: May 31, 2019
*) Corresponding author:
E-mail: [email protected]
ABSTRACT
Arthropods biodiversity on a rice ecosystem plays an important role related to the pest management. This research aimed to investigate the diversity and community structure of arthropods in the rice ecosystem. It was conducted in Lembah Seulawah, Aceh Besar Regency, Indonesia from February to August 2016. Sweep net was used to collect insects on four rice plots at 35, 45 and 55 days after transplanting (DAT) as vegetative, transition and generative stages respectively. The result showed that the twenty-five morpho-species found at vegetative stage was the highest among the three stages.
They were categorized as phytophagous insects, spiders, predatory insects, parasitoid, and neutral insects. Each arthropod’s category the highest among the three stages was in the higher abundance at vegetative stage, except for phytophagous arthropod.
The Shannon-Wiener diversity index (H’) was significantly higher at vegetative stage than those at remaining stages, while Simpson Dominance (C) and Species Evenness (E) indices were not significantly different among the three observed stages.
ISSN: 0126-0537 Accredited First Grade by Ministry of Research, Technology and Higher Education of The Republic of
Diversity and Community Structure of Arthropods on Rice Ecosystem in Aceh
J. Jauharlina *), H. Hasnah and M. Ikram Taufik
Faculty of Agriculture, Universitas Syiah Kuala, Banda Aceh, Indonesia
There have been many studies conducted to preserve beneficial organisms such as natural enemies which can be used as biological control agents (Ovawanda, Witjaksono, & Trisyono, 2016;
Sanda & Sunusi, 2014). These natural enemies (predators and parasitoids) instinctively can also play an important role in regulating the pest population.
Therefore, the maintenance of biodiversity, including predator and parasitoid, within the rice ecosystem is important to enhance their role in natural control or as biological control agents (Ueno, 2013). After rice establishment, arthropod species colonize and increase diversity progressively. Their communities may vary with the environment, cropping patterns, varieties and cultivation practices.
Biodiversity refers to the species variety or number present in an area or ecosystem (Price, Denno, Eubanks, Finke, & Kaplan, 2011). Rice fields often support high levels of biodiversity and play important role in the systems of agricultural productivity. An important aspect of IPM is to enhance natural control in the rice plantation, therefore, the presence of various species of arthropods and their population ecology are important things to be considered when designing pest management methods. The arthropod community in rice fields is known to have different ecological roles; they include pests, natural enemies (predators and parasitoids), saprophytes and aquatic arthropods.
These different groups can perform a stability in rice field ecosystem (Luo, Fu, & Traore, 2014). Many studies in Asia have shown that when the use of pesticides was reduced to conserve the predator communities, the destruction of rice plantation by the insect pests such as N. lugens decreased (Thorburn, 2015).
One of the major limitations in promoting natural and biological controls as part of IPM strategies is that not many farmers realize the role of arthropod groups found in their rice fields. They cannot differentiate pests from beneficial organisms, and they often just apply pesticide when they see species of arthropods in the rice field. Aceh Besar Regency is one of the centers for rice production in Aceh Province. Based on our preliminary interview with the rice farmers in this area, most of them think that any insect or other arthropods found on the rice plantation are pests that damage the plants. The fact that some of the arthropod groups are beneficial in regulating pest populations is new information for them. This research was conducted to identify
arthropod species and to investigate the diversity and community structure of arthropods on the conventional rice ecosystem grown by local farmers.
The results can be used in assessing conservation plan of natural enemies on the rice ecosystem in order to promote natural and biological controls as part of IPM approach.
MATERIALS AND METHODS Arthropod Samplings
The research took place in Lembah Seulawah District, Aceh Besar Regency from February to August 2016. The research site was one of rice production area in Aceh Province, having an altitude of 360 m above sea level. The arthropod samples were taken by using sweep nets from four plots that belong to local farmers in two nearby villages. The plots size ranged from 1500 m2 up to 3400 m2 (Table 1). All rice fields in this area were surrounded by secondary forest ecosystem consisting different species of plants. The same variety of rice (Inpari-36) was planted in each plot.
There was no particular treatment applied to the plots. Rice cultivation was employed as commonly practiced by the farmers. In this area, pesticides application was quite high, ranged from two to four times during the rice plantation.
This research was conducted from February to August 2016. The samplings were done between 07.00 – 10.00 a.m. using a sweep net on at least 10
% of plot size consisting five sub-areas in each plot.
The five sub-areas were selected in a diagonal way, four on the outer sides and one in the middle of each plot. The samples were collected at least one meter from the edge of each plot in order to reduce edge effects. The arthropod samples were taken mainly the ones flying above and near the surface of the rice plantation. The arthropods were sampled three times i.e. at 35, 45, and 55 days after transplanting (DAT) as representation of vegetative, transition, and generative stages of rice growth respectively.
All sampled arthropods were kept in plastic bottles containing 70 % ethanol and were brought to the Biological Control Laboratory, Agricultural Faculty, Syiah Kuala University for further identification.
The collected arthropods were then classified into five groups: phytophagous insects (pests), spiders, predatory insects, parasitoid, and neutral insects.
Individual number of each Arthropod category was calculated to define its population.
Data Analysis
The differences among the number of individual arthropods based on different functional groups were analyzed by using Analysis of Variance (ANOVA of logarithmic data). Means were separated with the Tukey-test when ANOVA showed any significant difference (P < 0.05). The diversity indices of the arthropod at the three stages of rice growth was calculated using Shannon-Wiener diversity index (H’), Species Evenness index (E), and the Simpson dominance index (C) (Tarno, Septia, & Aini, 2016). Analysis was done using R program version 3.3.1 (R. Core Team, 2016). The diversity indices were analyzed by using R program with Vegan package (Oksanen, 2019).
RESULTS AND DISCUSSION Species Richness and Abundance
In total, there were 2454 individuals of arthropods collected during the three stages of rice plantation.
They belonged to two classes, nine orders, 20 families and 25 morpho-species. The morpho-species and corresponding taxa of the specimens collected are shown in Table 1. The number of species found at vegetative stage of rice plantation (25 species) is higher than those on transition and generative stages of the plantation (16 species each) (Table 2). The species richness of arthropods in the rice plantation depends on the location of study, cultivation technique, and sampling methods (Zhang et al., 2013). In South Kalimantan, earlier study has shown that the number of species and their abundance are higher in the rice field that were received an IPM cultivation than those in the non-IPM. The number Arthropods species found was more than 50 species in IPM system of rice field.
However, the arthropod samples in the study were caught by using four kinds of trap: yellow sticky, light trap traps, insect nets and pitfall trap (Samharinto, Abadi, Raharjo, & Halim, 2012). In this research sites, pesticides were used 2-4 times during the rice growth
in each plot of the study. Besides, the arthropods samples were taken using one method only (sweep nets). It means that the arthropods caught in this study were only the ones flew over the rice plantation or the ones found on the surface of rice plantation.
The arthropods that were deep in the plantation or staying in the ground might have been missed. These two factors might contribute to less species richness in the area compared to those found in earlier study.
Pesticides have been known as one of major factors affecting biological diversity with serious negative impacts on pollinators, other invertebrates, amphibians and birds. In a short term, pesticide may have toxic effects to directly exposed organisms, or in a long term they may cause changes in habitat and food chains (Chagnon et al., 2015).
Three species of predators were always caught from each plot, namely Tetragnatha maxillosa (Araneae: Tetragnathidae), Agriocnemis femina (Odonata: Coenagrionidae), and Verania lineata (Coleoptera: Cocinelidae). These three species are known as general predators. The availability of their prey in all stages of rice growth probably had maintained their population in the field. Spiders have been known as important natural enemies of pests and also as indicators of biodiversity in rice field ecosystems (Betz & Tscharntke, 2017; Tanaka, 2016). Tetragnatha maxillosa is a spider species that is very active during the night and preys upon brown plant hopper (N.
lugens), leaf hopper (Nephotetteix spp.) and some other insect pest species (Betz & Tscharntke, 2017).
Spider diversity is significantly dependent on vegetation structure (Landsman & Bowman, 2017). The species richness and abundance of spiders are higher in the abandoned fields in which more plant species grown than in rice fields (Baba, Tanaka, & Kusumoto, 2019).
More species of spiders and/or more numbers might have occurred in the lower levels of the rice vegetation or at the base of the tillers. They might be missed by insect net that was used in this study.
Table 1. Rice plantation plots that were used as the sampling sites in Lembah Seulawah District, Aceh Besar Regency
Village Plot Number Plot Size Location Coordinates
East North
Lon Baroeh Plot 1 3400 m² 95⁰66’109’’ 5⁰35’952’’
Plot 2 3000 m² 95⁰66’280’’ 5⁰36’194’’
Lon Asan Plot 3 1700 m² 95⁰66’493’’ 5⁰35’829’’
Plot 4 1500 m² 95⁰66’73’’ 5⁰35’762’’
Table 2. The morpho-species and corresponding taxa of arthropods were collected from Lembah Seulawah District, Aceh Besar Regency, Aceh Province (Morpho-species data from four plots were combined overall and the same species that were sampled in more than one plot were counted once)
Rice field stage Order Family Morpho-species Category
Vegetative Araneae Tetragnathidae Tetragnatha maxillosa Spider
Araneidae Araneus inustus Spider
Linypidae Atypena formosana Spider
Oxyopidae Oxypes javanus Spider
Coleoptera Coccinellidae Verania lineata Predatory insect Micraspis crocea Predatory insect Carabidae Ophionea nigrofasciata Predatory insect Odonata Coenagrionidae Agriocnemis femina Predatory insect Agriocnemis pygmea Predatory insect Libellulidae Diplocodes trivialis Predatory insect Orthoptera Tettigonidae Conocephalus longipennis Predatory insect Gryllidae Metioche vittaticollis Predatory insect
Acrididae Oxya chinensis Phytophagous insect*
Valanga nigricornis Phytophagous insect*
Hemiptera Coreidae Leptocorisa oratorius Phytophagous insect*
Homoptera Cicadellidae Nephotettix virescens Phytophagous insect * Lepidoptera Pyralidae Cnaphalocrosis medinalis Phytophagous insect*
Scirphophaga innotata Phytophagous insect*
Hymenoptera Braconidae Apanteles sp. Parasitoid
Macrocentrus philippinensis Parasitoid
Ichneumonidae Tryphon sp. Parasitoid
Xanthopimpla flavolineata Parasitoid
Diptera Tachinidae Gonia picea Parasitoid
Pipunculidae Pipunculus mutillatus Parasitoid
Colicidae Culex sp. Neutral insect
Transition Araneae Araneidae Araneus inustus Spider
Tetragnathidae Tetragnatha maxillosa Spider
Linypidae Atypena formosana Spider
Coleoptera Coccinelidae Verania lineata Predatory insect
Carabidae Ophionea nigrofasciata Predatory insect Odonata Coenagriocnidae Agriocnemis femina Predatory insect Agriocnemis pygmea Predatory insect Orthoptera Tettigonidae Conocephalus longipennis Predatory insect Gryllidae Metioche vittaticollis Predatory insect
Hemiptera Coreidae Leptocorisa oratorius Phytophagous insect*
Homoptera Cicadellidae Nephotettix virescens Phytophagous insect*
Lepidoptera Pyralidae Cnaphalocrocis medinalis Phytophagous insect * Hymenoptera Braconidae Macrocentrus philippinensis Parasitoid
Diptera Tachnidae Gonia picea parasitoid
Pipunculidae Pipunculus mutillatus parasitoid Generative Araneae Tetragnathidae Tetragnatha maxillosa Spider
Coenagriocnidae Araneus inustus Spider
Odonata Coenagriocnidae Agriocnemis femina Predatory insect Coenagriocnidae Agriocnemis pygmea Predatory insect
Coleoptera Coccinelidae Verania lineata Predatory insect
Carabidae Ophionea nigrofasciata Predatory insect
Hymenoptera Braconidae Apanteles sp. Parasitoid
Diptera Tachnidae Gonia picea Parasitoid
Orthoptera Carabidae Conocephalus longipennis Predatory insect Gryllidae Metioche vittaticollis Predatory insect
Acrididae Oxya chinensis Phytophagous insect*
Valanga nigricornis Phytophagous insect*
Hemiptera Coreidae Leptocorisa oratorius Phytophagous insect*
Pantatomidae Nezara viridula Phytophagous insect*
Homoptera Cicadellidae Nephotettix virescen Phytophagous insect*
Lepidoptera Pyralidae Scirphopaga innotata Phytophagous insect*
Agriocnemis femina is a small damselfly that consumes other small insects while V. lineata is a predator species that mostly consumes brown plant hopper and leaf hopper (Siregar, Md. Rawi, Ahmad,
& Nasution, 2016). Culex sp. (Diptera: Colicidae) was abundance at vegetative stage of rice growth and none of them was found at other stages. The watery rice field in earlier stage of plantation was a suitable site for larval development of Culex sp.
Mean number of individual arthropods collected per plot based on different functional categories are presented in Table 3. The number of species across each category varied greatly and almost all categories had higher number of individuals at vegetative stage of rice growth, except for phytophagous insect. All phytophagous insects found were known as pests on rice plantation. This study showed that the abundance of phytophagous insects was higher significantly (F = 8.31, P = 0.009) at generative stage of rice growth than at transition and vegetative stages. The high frequency of pesticide application on the research sites might decrease the other arthropods abundance at later stages of rice plantation (Ueno, 2013). The number of collected spiders at vegetative stage was significantly higher (F = 9.74, P =0.005) than both transition and generative stages. However, in the
three stages of rice growth, the difference among the numbers of predatory insects was not significant (F = 1.65, P =0.24).
Species Diversity and Dominance
The Shannon-Wiener diversity index (H’) is significantly higher at vegetative stage of rice growth (F = 4.66, P = 0.04) than those at both transition and generative stages (Table 4). However, all stages were categorized as low diversity because the individual distribution for each species was at the low level. Tarno, Septia, & Aini (2016) stated that the value of Shannon-Wiener diversity index (H’) when less than 1 is categorized as low diversity and low individual distribution of each species. The Simpson Dominance index (C) (F = 3.91, P = 0.06) were not significantly different among the three stages of rice growth and all of stages were categorized in middle dominance species. Tarno, Septia, & Aini (2016) stated that the value of Simpson Dominance index (C) in 0.50 < C < 0.75 is categorized as middle dominance of species. The Species Evenness index (E) (F = 2.45, P = 0.14) also showed not significantly different among the three stages of rice growth. All of stages were categorized in low evenness species.
Tarno, Septia, & Aini (2016) stated that the value of Species Evenness index < 0.05 showed that evenness is low and community is under pressure.
Table 3. Mean number of individual arthropods caught (Mean ± SE) per plot based on different functional groups from three different stages of rice growth in Lembah Seulawah District, Aceh Besar Regency, Aceh Province
Stage of Rice
Growth Phytophagous
insects Spiders Predatory
insects Neutral insects Parasitoid insects Vegetative 28.00 ± 5.13 a 80.00 ± 19.58 a 62.00 ± 13.93 a 189.00 ±157.00 25.00 ± 13.86 Transition 17.00 ± 7.33 a 18.00 ± 5.94 b 65.00 ± 10.55 a 0.00 ± 0.00 3.00 ± 2.50 Generative 80.00 ± 11.66 b 7.00 ± 4.57 b 39.00 ± 8.32 a 0.00 ± 0.00 1.00 ± 0.50 Remarks: *Mean values within a column followed by the same letter shows there are no significantly different by Tukey HSD at α < 0.05.
Table 4. Diversity indices of arthropods were (Mean ± SE) calculated from four plots in different stages of rice growth in Lembah Seulawah District, Aceh Besar Regency, Aceh Province
Stages of rice growth Diversity index
Shannon-Wiener (H´) Simpson Dominance (C) Species Evenness (E)
Vegetative 0.88 ± 0.11 a 0.51 ± 0.06 a 0.31 ± 0.03 a
Transition 0.47 ± 0.11 b 0.72 ± 0.08 a 0.21 ± 0.05 a
Generative 0.67 ± 0.01 b 0.54 ± 0.01 a 0.31 ± 0.01 a
Remarks: *Mean values within a column followed by the same letter shows there are no significantly different by Tukey HSD at α < 0.05
The diversity of arthropod community varies greatly in different seasons and at rice growth stages (Zhang et al., 2013). The results in the present study showed that the three indices varied across different stages of rice growth, even though only the Shannon-Wiener index (H’) was significantly different.
The composition of species based on each functional category showed a different trend at the three stages of rice growth. Based on the proportion of species abundance, 63% of total individual numbers of arthropods was collected at vegetative stage of rice growth and 21% and 16% were at transition and at generative stages respectively. However, the distribution of each functional category at vegetative stage was quite homogenous compared to the distribution at transition and generative stages (Fig.
1). At transition stage, arthropod community was dominated by predatory insects (64%) while at generative stage was dominated by phytophagous insects (63%). The availability of neutral insect was the highest (30%) at vegetative stage of rice growth.
The presence of this neutral insect at earlier stage of rice growth may cause higher composition of predatory insects at transition stage. The neutral
species has been known to play an important role in the community food web in rice fields (Zhang et al., 2013).
The predatory insect found at transition stage of rice growth was dominated by the species Verania lineata (Coeloptera: Coccinellidae), while the majority of phytophagous insects collected at generative stage was the species Leptocorisa oratorius (Hemiptera: Coreidae). The high density of the species L. oratorius corresponded to the stage of rice growth. The samplings for generative stage of rice were done at 55 DAT, the stage where the rice plantation just formed panicles and their content were still soft. This stage of rice growth was very much attractive to the species L. oratorius which feeds on the sap of the panicles rice. The rice bug L. oratorius is a conspicuous and a common insect that emits a strong odor. Leptocorisa oratorius is the species associated with lowland rice in Indonesia (As’ad, Kaidi, & Syarief, 2018). This research has shown that despite of using pesticide by local farmers in their field rice, natural enemies especially predators were still exist. Their presence in rice fields can be used to enhance natural control and to reduce the pesticide application.
Fig. 1. Composition of each functional category of Arthropods were sampled from four plots in different stages of rice growth in Lembah Seulawah District, Aceh Besar Regency, Aceh Province
CONCLUSION AND SUGGESTION
This research showed that all collected arthropods were categorized as phytophagous insects, spiders, predatory insects, parasitoid, and neutral insects. There were 25 morpho species found at vegetative stage representing the highest number among the three stages. Each arthropod’s category was in the higher abundance at vegetative stage, except for phytophagous arthropod.
The Shannon-Wiener diversity index (H’) was significantly higher at vegetative stage than those at the remaining stages, while Simpson Dominance index (C) and Species Evenness (E) indices were not significantly different among the three observed stages. The species richness found was quite varied, however there were several common species found in each sampled plot, namely Tetragnatha maxillosa (Araneae: Tetragnathidae), Agriocnemis femina (Odonata: Coenagrionidae), and Verania lineata (Coleoptera: Cocinelidae). The presence of these general predators may play an important role to control the pest population in the observed rice field.
ACKNOWLEDGEMENT
The authors would like to thank Afriyani (the technician in the Biological Control Laboratory of Agricultural Faculty, Syiah Kuala University) for preparing the microscope used in specimen identification and assisting in keeping the specimens in the laboratory.
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